Skip to main content
SpringerLink
Log in

BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Pectin methylesterase (PME) is known to have important roles in pollen development and pollen tube growth. As pivotal regulatory factors in PME activity modulation, PME inhibitors (PMEIs) are thought to be key regulators of cell wall stability at the tip of the pollen tube. We report on the cloning and characterization of a novel B. oleracea PMEI gene, BoPMEI1. Heterologously expressed BoPMEI1 showed PMEI activity. RT-PCR studies of different tissues and promoter-GUS fusions confirmed that BoPMEI1 was specifically expressed in mature pollen grains and pollen tubes. Based on in vivo transient assays, we found that BoPMEI1 appears to be largely localized to the plasma membrane. Transgenic Arabidopsis plants expressing antisense BoPMEI1 under the control of the CaMV 35S promoter suppressed the expression of the orthologous gene At1g10770, which led to partial male sterility and decreased seed set by inhibition of pollen tube growth. Our study demonstrates the involvement of BoPMEI1 in pollen tube growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

PME:

Pectin methylesterase

PMEI:

Pectin methylesterase inhibitor

RT-PCR:

Reverse transcriptase polymerase chain reaction

CaMV:

35S Cauliflower mosaic virus 35S

GUS :

Beta-glucuronidase

cDNA-AFLP:

cDNA-amplified fragment length polymorphism

ORF:

Open reading frame

kDa:

Kilometer Dalton

nt:

Nucleotide

aa:

Amino acid

IPTG:

Isopropyl β-D-1-thiogalactopyranoside

Kan:

Kanamycin

GFP:

Green-fluorescent protein

References

  • An SH, Sohn KH, Choi HW, Hwang IS, Lee SC, Hwang BK (2008) Pepper pectin methylesterase inhibitor protein CaPMEI1 is required for antifungal activity, basal disease resistance and abiotic stress tolerance. Planta 228:61–78

    Article  CAS  PubMed  Google Scholar 

  • Andersson J, Walters RG, Horton P, Jansson S (2001) Antisense inhibition of the photosynthetic antenna proteins CP29 and CP26: implications for the mechanism of protective energy dissipation. Plant Cell 13:1193–1204

    Article  CAS  PubMed  Google Scholar 

  • Balestrieri C, Castaldo D, Giovane A, Quagliuolo L, Servillo L (1990) A glycoprotein inhibitor of pectin methylesterase in kiwi fruit (Actinidia chinensis). Eur J Biochem 193:183–187

    Article  CAS  PubMed  Google Scholar 

  • Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725

    Article  CAS  PubMed  Google Scholar 

  • Bosch M, Hepler PK (2006) Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta 223:736–745

    Article  CAS  PubMed  Google Scholar 

  • Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346

    Article  CAS  PubMed  Google Scholar 

  • Camardella L, Carratore V, Ciardiello MA, Servillo L, Balestrieri C, Giovane A (2000) Kiwi protein inhibitor of pectin methylesterase amino-acid sequence and structural importance of two disulfide bridges. Eur J Biochem 267:4561–4565

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, Cervone F, Bellincampi D, Tsernoglou D (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17:849–858

    Article  CAS  PubMed  Google Scholar 

  • Fan LM, Wang YF, Wang H, Wu WH (2001) In vitro Arabidopsis pollen germination and characterization of the inward potassium currents in Arabidopsis pollen grain protoplasts. J Exp Bot 52:1603–1614

    Article  CAS  PubMed  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, Preuss D (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12:2001–2008

    Article  CAS  PubMed  Google Scholar 

  • Francis KE, Lam SY, Copenhaver GP (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiol 142:1004–1013

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, Morvan C, Roland JC (1986) Composition, properties and localization of pectins in young and mature cells of the mung bean hypocotyls. Plant Cell Physiol 27:417–429

    CAS  Google Scholar 

  • Grant GT, Morris ER, Rees DA, Smith PJC, Thom D (1973) Biological interactions between polysaccharides and divalent cations: the egg-box model. FEBS Lett 32:195–198

    Article  CAS  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85

    Article  PubMed  Google Scholar 

  • Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell 16:3437–3447

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  Google Scholar 

  • Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596

    Article  CAS  PubMed  Google Scholar 

  • Kang J, Zhang G, Bonnema G, Fang Z, Wang X (2008) Global analysis of gene expression in flower buds of Ms-cd1 Brassica oleracea conferring male sterility by using an Arabidopsis microarray. Plant Mol Biol 66:177–192

    Article  CAS  PubMed  Google Scholar 

  • Krichevsky A, Kozlovsky SV, Tian GW, Chen MH, Zaltsman A, Citovsky V (2007) How pollen tubes grow. Dev Biol 303:405–420

    Article  CAS  PubMed  Google Scholar 

  • Latijnhouwers M, Hawes C, Carvalho C, Oparka K, Gillingham AK, Boevink P (2005) An Arabidopsis GRIP domain protein locates to the trans-Golgi and binds the small GTPase ARL1. Plant J 44:459–470

    Article  CAS  PubMed  Google Scholar 

  • Levitan A, Danon A, Lisowsky T (2004) Unique features of plant mitochondrial sulfhydryl oxidase. J Biol Chem 279:20002–20008

    Article  CAS  PubMed  Google Scholar 

  • Li Y-Q, Mareck A, Faleri C, Moscatelli A, Liu Q, Cresti M (2002) Detection and localization of pectin methyl esterase isoforms in pollen tubes of Nicotiana tabacum L. Planta 214:734–740

    Article  CAS  PubMed  Google Scholar 

  • Lou P, Kang JG, Zhang GY, Bonnema G, Fang ZY, Wang XW (2007) Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119

    Article  CAS  Google Scholar 

  • Louvet R, Cavel E, Gutierrez L, Guenin S, Roger D, Gillet F, Guerineau F, Pelloux J (2006) Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta 224:782–791

    Article  CAS  PubMed  Google Scholar 

  • Markovic O, Janecek S (2004) Pectin methylesterases: sequence-structural features and phylogenetic relationships. Carbohydr Res 339:2281–2295

    Article  CAS  PubMed  Google Scholar 

  • Mascarenhas JP (1989) The male gametophyte of flowering plants. Plant Cell 1:657–664

    Article  PubMed  Google Scholar 

  • Micheli F (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci 6:414–419

    Article  CAS  PubMed  Google Scholar 

  • Nelson BK, Cai X, Nebenfuhr A (2007) A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 51:1126–1136

    Article  CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  CAS  PubMed  Google Scholar 

  • Pelloux J, Rusterucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  CAS  PubMed  Google Scholar 

  • Pih KT, Yi MJ, Liang YS, Shin BJ, Cho MJ, Hwang I, Son D (2000) Molecular cloning and targeting of a fibrillarin homolog from Arabidopsis. Plant Physiol 123:51–58

    Article  CAS  PubMed  Google Scholar 

  • Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  CAS  PubMed  Google Scholar 

  • Raiola A, Camardella L, Giovane A, Mattei B, De Lorenzo G, Cervone F, Bellincampi D (2004) Two Arabidopsis thaliana genes encode functional pectin methylesterase inhibitors. FEBS Lett 557:199–203

    Article  CAS  PubMed  Google Scholar 

  • Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. BBA Proteins Proteomics 1696:253–261

    Article  CAS  Google Scholar 

  • Ravanel S, Cherest H, Jabrin S, Grunwald D, Surdin-Kerjan Y, Douce R, Rebeille F (2001) Tetrahydrofolate biosynthesis in plants: molecular and functional characterization of dihydrofolate synthetase and three isoforms of folylpolyglutamate synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 98:15360–15365

    Article  CAS  PubMed  Google Scholar 

  • Rockel N, Wolf S, Kost B, Rausch T, Greiner S (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J 53:133–143

    Article  PubMed  Google Scholar 

  • Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale DM, Twell D (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45:577–585

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto W, Zaltsman A, Adam Z, Takahashi Y (2003) Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15:2843–2855

    Article  CAS  PubMed  Google Scholar 

  • Sanders BuiA, Wetering K, McIntire K, Hsu Y, Lee P, Truong M, Beals T, Goldberg R (1999) Anther developmental defects in Arabidopsis thaliana male sterile mutants. Sex Plant Reprod 11:297–322

    Article  CAS  Google Scholar 

  • Scognamiglio MA, Ciardiello MA, Tamburrini M, Carratore V, Rausch T, Camardella L (2003) The plant invertase inhibitor shares structural properties and disulfide bridges arrangement with the pectin methylesterase inhibitor. J Protein Chem 22:363–369

    Article  CAS  PubMed  Google Scholar 

  • Sumie I, Akiko K, Junichi U, Ikuo N, Kiyotaka O (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 10:2191–2210

    Google Scholar 

  • Tian GW, Chen MH, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83–91

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Grsic-Rausch S, Rausch T, Greiner S (2003) Identification of pollen-expressed pectin methylesterase inhibitors in Arabidopsis. FEBS Lett 555:551–555

    Article  CAS  PubMed  Google Scholar 

  • Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1540

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was conducted at the Key Opening Laboratory of Vegetable Genetics and Physiology funded by the Chinese Ministry of Agriculture and the Sino-Dutch Joint Plant Genome Analysis Laboratory at the Institute of Vegetables and Flowers (CAAS). The work was supported by National Natural Science Foundation projects 30370981, 30471188 and 30400298.

Author information

Authors and Affiliations

  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, 12 Zhongguancun Nandajie, Beijing, 100081, People’s Republic of China

    Guo Yu Zhang, Jing Feng, Jian Wu & Xiao Wu Wang

Authors
  1. Guo Yu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jing Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jian Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiao Wu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiao Wu Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, G.Y., Feng, J., Wu, J. et al. BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta 231, 1323–1334 (2010). https://doi.org/10.1007/s00425-010-1136-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1136-7

Keywords

Search

Navigation